A War of Tiny Giants - Do viruses impact Pelagibacterales genotype dynamics in the Western English Channel

小巨人之战 - 病毒会影响西英吉利海峡的海洋杆菌基因型动态吗

• 批准号: NE/R010935/1
• 负责人: Ben Temperton
• 金额: $ 80.35万
• 依托单位: UNIVERSITY OF EXETER
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2018
• 资助国家: 英国
• 起止时间: 2018 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FR010935%2F1
• 关键词: War; Tiny; Giants; Do; viruses

One often hears that the rainforests are the 'lungs of the Earth', producing the oxygen that we breathe through photosynthesis and drawing down atmospheric carbon dioxide. However, perhaps less well-known is the fact that the oceans, and in particular coastal regions, are responsible for about half of all global photosynthesis as marine bacteria and algae (known as phototrophs) capture sunlight to produce metabolites for growth. Through cell death and the leaky nature of cell walls, products of photosynthesis find their way into the water, where they are consumed by other bacteria (known as heterotrophs), releasing the captured carbon dioxide back to the atmosphere. Perhaps the most important group of heterotrophs is the Pelagibacterales. These tiny cells dominate global oceans (up to 500,000 in every mL of seawater) and are responsible for converting up to 40% of marine photosynthetic products back to atmospheric CO2. As a result, they have a major impact on global carbon cycling and can be considered global bioengineers. For over a decade we have been studying how nutrient availability in the oceans drive Pelagibacterales ecology and evolution, in a bid to build better models of future global carbon cycling under the influences of climate change. As oceans warm and nutrients become less available, Pelagibacterales abundance, and their importance in carbon cycling, is set to increase further. However, not every member of the Pelagibacterales is equal - they differentiate into distinct ecological niches (known as 'ecotypes') with different capacities to take up resources and release important climate-changing gases such as methane and dimethylsulfide. Therefore, understanding which conditions favour which type of Pelagibacterales is of major importance for climate modelling.Perhaps the only organisms on Earth more important to global carbon cycles than the Pelagibacterales are the viruses that infect them. Based on their extraordinary abundance and diversity, J.B.S. Haldane once quipped that 'The Creator would appear as endowed with a passion for stars, on the one hand, and for beetles on the other'. In comparison, the Creator's zeal for viruses would make stars and beetles appear to be a side-project performed with perfunctory indifference. Virus numbers are staggering - they are by far the most abundant and diverse organisms on Earth. If one assumes that there are 10 trillion galaxies in the universe and each one is similar to our Milky Way and contains 100 billion stars, then the oceans are populated with a million viruses for every star in the universe. Of these, the vast majority are viruses that infect and kill bacteria (known as 'phages'), and of these, around a quarter are thought to infect Pelagibacterales. Yet, until 2013, the existence of viruses that infect Pelagibacterales was entirely unknown! Similar to interactions between lions and wildebeest in the Serengeti, predation is rather unfortunate for the host, but provides benefits to the scavengers of the ecosystem. Phage-induced cell death releases the contents of the host cell into the water column and this soup of dissolved organic matter provides nutrients to surviving cells. Furthermore, like the arms-race between lions and wildebeest (bigger claws, horns etc.), bacteria and viruses co-evolve to produce resistance and counter-resistance mechanisms. In some cases, this co-evolution can lead to the emergence of new types of host, resistant to viruses and capable of thriving despite high viral abundance. Therefore, both nutrients and viral predation can influence the abundance and diversity of marine bacteria. This project is the first attempt to evaluate the impact of the viruses infecting Pelagibacterales on their diversity and abundance over seasonal timescales. The findings will enable us to build better models of future carbon biogeochemistry by accurately incorporating viral predation of the Pelagibacterales in global carbon cycling.

人们经常听说雨林是“地球之肺”，通过光合作用产生我们呼吸的氧气，并吸收大气中的二氧化碳。然而，也许不太为人所知的是，海洋，特别是沿海地区，负责大约一半的全球光合作用，因为海洋细菌和藻类（称为光养生物）捕获阳光以产生生长代谢物。通过细胞死亡和细胞壁的渗漏性质，光合作用的产物进入水中，在那里它们被其他细菌（称为异养生物）消耗，将捕获的二氧化碳释放回大气。也许最重要的异养生物群是Pelagiophales。这些微小的细胞主宰着全球海洋（每毫升海水中多达50万个），负责将高达40%的海洋光合产物转化为大气中的二氧化碳。因此，它们对全球碳循环产生重大影响，可以被视为全球生物工程师。十多年来，我们一直在研究海洋中的营养物质是如何驱动Pelagiorales生态和进化的，以建立更好的气候变化影响下未来全球碳循环模型。随着海洋变暖和营养物质变得越来越少，Pelagiesales丰度及其在碳循环中的重要性将进一步增加。然而，并不是每一个Pelagiorales的成员都是平等的-它们分化成不同的生态位（称为“生态型”），具有不同的能力来吸收资源并释放重要的气候变化气体，如甲烷和二甲基硫。因此，了解哪种条件有利于哪种类型的Pelagiorales对气候建模至关重要。也许地球上唯一比Pelagiorales对全球碳循环更重要的生物是感染它们的病毒。基于它们异常丰富和多样性，J.B.S. Halfman曾经打趣说，“造物主似乎一方面对星星充满热情，另一方面又对甲虫充满热情。相比之下，造物主对病毒的热情会使恒星和甲虫看起来像是一个敷衍冷漠的附带项目。病毒数量惊人--它们是迄今为止地球上最丰富、最多样化的生物。如果假设宇宙中有10万亿个星系，每个星系都与我们的银河系相似，包含1000亿颗恒星，那么宇宙中每有一颗星星，海洋中就有一百万个病毒。其中，绝大多数是感染和杀死细菌的病毒（称为“噬菌体”），其中约四分之一被认为感染了Pelagiorales。然而，直到2013年，感染Pelagiorales的病毒的存在是完全未知的！与塞伦盖蒂的狮子和角马之间的相互作用类似，捕食对宿主来说是相当不幸的，但却为生态系统的食腐动物提供了好处。噬菌体诱导的细胞死亡将宿主细胞的内容物释放到水柱中，这种溶解的有机物汤为存活的细胞提供营养。此外，就像狮子和角马之间的军备竞赛（更大的爪子，角等），细菌和病毒共同进化以产生耐药性和反耐药性机制。在某些情况下，这种共同进化可能导致新类型宿主的出现，这些宿主对病毒具有抵抗力，并且能够在病毒丰度很高的情况下蓬勃发展。因此，营养物质和病毒捕食都可以影响海洋细菌的丰度和多样性。该项目是第一次尝试评估感染Pelagiorales的病毒在季节性时间尺度上对其多样性和丰度的影响。这些发现将使我们能够通过准确地将Pelagiorales的病毒捕食纳入全球碳循环来建立未来碳地球化学的更好模型。

项目成果

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

• DOI: 10.1101/2020.04.17.046896
• 发表时间: 2020-04
• 期刊: bioRxiv
• 作者: Michael W. Henson;V. C. Lanclos;D. Pitre;J. Weckhorst;Anna M. Lucchesi;Chuankai Cheng;B. Temperton;J. C. Thrash

Efficient dilution-to-extinction isolation of novel virus-host model systems for fastidious heterotrophic bacteria.

• DOI: 10.1038/s41396-020-00872-z
• 发表时间: 2021-06
• 期刊: The ISME journal
• 作者: Buchholz HH;Michelsen ML;Bolaños LM;Browne E;Allen MJ;Temperton B
• 通讯作者: Temperton B

Efficient Dilution-to-Extinction isolation of novel virus-host model systems for fastidious heterotrophic bacteria

苛求异养细菌的新型病毒宿主模型系统的有效稀释至灭绝分离

• DOI: 10.1101/2020.04.27.064238
• 发表时间: 2020
• 作者: Buchholz H

A Novel and Ubiquitous Marine Methylophage Provides Insights into Viral-Host Coevolution and Possible Host-Range Expansion in Streamlined Marine Heterotrophic Bacteria.

• DOI: 10.1128/aem.00255-22
• 发表时间: 2022-04-12
• 期刊: Applied and environmental microbiology
• 影响因子: 4.4

Influence of short and long term processes on SAR11 communities in open ocean and coastal systems.

• DOI: 10.1038/s43705-022-00198-1
• 发表时间: 2022-11-19
• 期刊: ISME COMMUNICATIONS
• 作者: Bolanos, Luis M.;Tait, Karen;Somerfield, Paul J.;Parsons, Rachel J.;Giovannoni, Stephen J.;Smyth, Timothy;Temperton, Ben
• 通讯作者: Temperton, Ben